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Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas?

Monogeneans (flatworms) are among the most host-specific of parasites in general and may be the most host-specific of all fish parasites. Specificity, in terms of a restricted spatial distribution within an environment, is not unique to parasites and is displayed by some fungi, insects, birds, symbionts and pelagic larvae of free-living marine invertebrates. The nature of cues, how "habitats" are recognised and how interactions between partners are mediated and maintained is of interest across these diverse "associations". We review some experiments that demonstrate important factors that contribute to host-specificity at the level of infective stages (larvae of oviparous monogeneans; juveniles of viviparous gyrodactylids) and adult parasites. Recent research on immune responses by fish to monogenean infections is considered. We emphasise the critical importance of host epidermis to the Monogenea. Monogeneans live on host epidermis, they live in its products (e.g. mucus), monopisthocotyleans feed on it, some of its products are "attractants" and it may be an inhospitable surface because of its immunological activity. We focus attention on fish but reference is made to amphibian hosts. We develop the concept for a potential role in host-specificity by the anterior adhesive areas, either the specialised tegument and/or anterior secretions produced by monogeneans for temporary but firm attachment during locomotion on host epithelial surfaces. Initial contact between the anterior adhesive areas of infective stages and host epidermis may serve two important purposes. (1) Appropriate sense organs or receptors on the parasite interact with a specific chemical or chemicals or with surface structures on host epidermis. (2) A specific but instant recognition or reaction occurs between component(s) of host mucus and the adhesive(s) secreted by monogeneans. The chemical composition of fish skin is known to be species-specific and our preliminary analysis of the chemistry of some monogenean adhesives indicates they are novel proteins that display some differences between parasite families and species.

Animals↗

Perch (Perca fluviatilis L.) parasites reflect ecosystem conditions: a comparison of a natural lake and two acidic reservoirs in Finland.

Parasite communities of perch were studied in a natural lake (Vetämäjärvi) and two reservoirs (the Kyrkösjärvi and Liikapuro reservoirs) located in Western Finland. All water bodies studied are small, shallow and humic. However, the reservoirs are more acidic than the lake (pH 5.9 and 5.3 vs. 6.4). Altogether, 18 parasite species were found, but the component communities were reduced in the harsh conditions of the reservoirs (12 and six species) as compared with the lake (17 species). In addition, the mean number of metazoan parasite specimens per fish was markedly lower in the reservoirs (64.3 and 14.3 specimens) than in the lake (116.1 specimens). Our prediction on the depauperation of parasite communities in reservoirs as compared with the lake was confirmed. Many ectoparasite groups were rare and most of the digenean parasites using molluscs as their intermediate host were absent from the reservoirs due to the inability of molluscs to tolerate the acidic water. The only digenean parasite found in the less acidic reservoir was Bunodera luciopercae. There were also species that preferred reservoirs as was expected. The protozoan ciliate Capriniana piscium benefiting acidic water and Acanthocephalus lucii, due to the abundance of its intermediate host, were most prevalent in the reservoir conditions.

Animals↗

Cell: sporozoite interactions and invasion by apicomplexan parasites of the genus Eimeria.

The site specificity that avian Eimeria sporozoites and, to a more limited degree, other apicomplexan parasites exhibit for invasion in vivo suggests that specific interactions between the sporozoites and the target host cells may mediate the invasion process. Although sporozoite motility and structural and secreted antigens appear to provide the mechanisms for propelling the sporozoite into the host cell,there is a growing body of evidence that the host cell provides characteristics by which the sporozoites recognise and interact with the host cell as a prelude to invasion. Molecules on the surface of cells in the intestinal epithelium, that act as receptor or recognition sites for sporozoite invasion, may be included among these characteristics. The existence of receptor molecules for invasion by apicomplexan parasites was suggested by in vitro studies in which parasite invasion was inhibited in cultured cells that were treated with a variety of substances designed to selectively alter the host cell membrane. These substance included cationic compounds or molecules, enzymes that cleave specific linkages, protease inhibitors, monoclonal antibodies, etc. More specific evidence for the presence of receptors was provided by the binding of parasite antigens to specific host cell surface molecules. Analyses of host cells have implicated 22, 31, and 37 kDa antigens, surface membrane glycoconjugates,conserved epitopes of host cells and sporozoites, etc., but no treatment that perturbs these putative receptors has completely inhibited invasion of the cells by parasites. Regardless of the mechanism,sporozoites of the avian Eimeria also invade the same specific sites in foreign host birds that they invade in the natural host. Thus, site specificity for invasion may be a response to characteristics of the intestine that are shared by a number of hosts rather than to a unique trait of the natural host. Protective immunity elicited against avian Eimeria species is not manifested in a total blockade of parasite invasion. In fact, the effect of immunity on invasion differs according to the eliciting species and depends upon the area of the intestine that is invaded. Immunity produced against caecal species of avian Eimeria, for example Eimeria tenella and Eimeria adenoeides, inhibits subsequent invasion by homologous or heterologous challenge species, regardless of the area of the intestine that the challenge species invade. Conversely, in birds immunised with upper intestinal species, Eimeria acervulina and Eimeria meleagrimitis, invasion by challenge species is not decreased and often is significantly increased.

Animals↗

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.

Animals↗

Nutritional adaptations to parasitism within the platyhelminthes.

Some of the most significant alterations to the basic turbellarian plan are evident in the adaptations that relate to the acquisition of food by parasitic flatworms, reflecting the most potent of selection pressures in initiating and maintaining the host-parasite association. Nutritionally, ectoparasitic monogeneans show most correspondence with the predatory turbellarians, with certain monopisthocotylean members feeding by means of a protrusible pharynx and extracorporeal digestion, as skin-browsers of fish, with extensive intracellular digestion involving lysosomal enzymes in a well-differentiated gut. The more sheltered vascularised gill chamber of fish provides many polyopisthocotylean monogeneans with a totally renewable and more comprehensive diet in the form of blood, but haematophagy has necessitated a number of digestive adaptations, not least in resolving the problem of intracellular accumulations of haematin pigment. Haematophagy is the predominant feeding strategy of digeneans, but in contrast to monogeneans digestion of blood is largely extracellular; in schistosomes digestion is rapid, involving a battery of cathepsin-like cysteine proteinases and aminopeptidases. The external surfaces of all parasitic flatworms depart from turbellarian character and are composed of a multifunctional syncytial tegument, which is permeable to a variety of small organic solutes, some crossing by passive diffusion, others via facilitated or active mediated transport. The relative roles of the tegument and gut in trematode nutrition are difficult to assess, but can be related to the nature of the microhabitat within the host. Cestodes are highly adapted intestinal parasites bereft of any vestige of gut, and their tegument has become elaborated into a sophisticated and highly efficient digestive-absorptive layer, rivalling the vertebrate mucosa in its ability to gain kinetic advantage in the selective uptake of nutrient at the host-parasite interface. The patterns of energy metabolism in adult flatworm parasites are generally anaerobic and based on glycogen, with abbreviated metabolic pathways and the loss of biosynthetic capacities.

Animal Nutritional Physiological Phenomena↗

Parasite body size distributions: interpreting patterns of skewness.

We examined the distributions of log body sizes of parasite species to test the prediction that the different physical constraints acting on endoparasites and ectoparasites can lead to different size distributions, and to see whether the distributions of parasite body sizes differ from those of free-living animals. We used body size distributions from 19 groups of parasitic of free-living animals, including over 7000 species and almost 2400 genera. There were differences between the body size distributions of male and female parasites, and between the body size distributions of related parasites exploiting different types of hosts. In general, parasite body size distributions were less frequently log right skewed than those of free-living animals. Ectoparasites tended to have more symmetric body size distributions than endoparasites, in which the most speciose size classes tended to be the smaller ones. Severe space constraints and a greater diversity of small niches may only allow the diversification of small endoparasites, whereas ectoparasite body sizes may face less severe limitations.

Animals↗

Control of parasites in cultured marine finfishes in Southeast Asia--an overview.

Mariculture in Southeast Asia began in the 1970s and expanded rapidly during the 1980s, with the commercial hatchery production of the seabass Lates calcarifer. Other important cultured species were Epinephelus coioides, Epinephelus malabaricus, Lutjanus johni, and Lutjanus argentimaculatus. Intensification in the polyculture of these species and the large-scale international movement of fingerlings or juveniles, as well as the rapid expansion and concentration of fish farms, have caused severe problems resulting from parasitic infections. Infections in maricultured fish are predominantly caused by monoxenous parasites, in particular the capsalid and diplectanid monogeneans. Heteroxenous blood parasites also successfully maintained transmission in the culture system despite their requirement for an intermediate host. Prophylactic chemical treatments helped to reduce parasitic infection but did not eliminate them and once introduced into the floating netcage culture system, these parasites managed to maintain their transmission successfully. Despite the current lack of information regarding the biology of many parasites affecting cultured marine fishes, it nevertheless is possible to develop methodologies to produce an integrated health management system specifically designed to the needs of the mariculture practiced in the Southeast Asian region. This system is important and should include a sequence of prophylaxes, adequate nutrition, sanitation, immunization and an effective system of marketing for farmed fishes.

Animals↗

Testing alternative hypotheses for variation in amphipod behaviour and life history in relation to parasitism.

We tested two hypotheses concerning changes in investment in current reproduction for parasitised hosts, using amphipods (Corophium volutator) which act as second intermediate hosts for trematodes (Gynaecoyla aduncta). One hypothesis requires that parasites exert control over their hosts (parasite manipulation), whereas the other predicts that hosts control decisions over investment (adaptive host response). Although these hypotheses are viewed as mutually exclusive, our various results support both hypotheses. For example, female amphipods infected by late-stage larvae were often found crawling at times when predation by sandpipers (Calidris pusilla), which are the final hosts for trematodes, was likely, while uninfected females typically remained in their burrows. Furthermore, old females that were newly-infected by trematodes often aborted and ate their young. Both of these responses seem inconsistent with female investment in current reproduction, but can be interpreted as adaptive parasite manipulation. In contrast, young non-ovigerous females that were newly-infected hastened the onset of their parturial moult and thus, time to becoming receptive. This response can be explained as a host adaptation to minimise the cost of parasites. We contend that differences between parasitised and unparasitised hosts in behaviour or investment can be explained as both parasite and host adaptations, expressed at different times in the host's life history. Such compromise will help explain the persistence of parasite-host associations in nature.

Adaptation, Physiological↗

Progress with parasite plastids.

This review offers a snapshot of our current understanding of the origin, biology, and metabolic significance of the non-photosynthetic plastid organelle found in apicomplexan parasites. These protists are of considerable medical and veterinary importance world-wide, Plasmodium spp., the causative agent of malaria being foremost in terms of human disease. It has been estimated that approximately 8% of the genes currently recognized by the malarial genome sequencing project (now nearing completion) are of bacterial/plastid origin. The bipartite presequences directing the products of these genes back to the plastid have provided fresh evidence that secondary endosymbiosis accounts for this organelle's presence in these parasites. Mounting phylogenetic evidence has strengthened the likelihood that the plastid originated from a red algal cell. Most importantly, we now have a broad understanding of several bacterial metabolic systems confined within the boundaries of the parasite plastid. The primary ones are type II fatty acid biosynthesis and isoprenoid biosynthesis. Some aspects of heme biosynthesis also might take place there. Retention of the plastid's relict genome and its still ill-defined capacity to participate in protein synthesis might be linked to an important house-keeping process, i.e. guarding the type II fatty acid biosynthetic pathway from oxidative damage. Fascinating observations have shown the parasite plastid does not divide by constriction as in typical plants, and that plastid-less parasites fail to thrive after invading a new cell. The modes of plastid DNA replication within the phylum also have provided surprises. Besides indicating the potential of the parasite plastid for therapeutic intervention, this review exposes many gaps remaining in our knowledge of this intriguing organelle. The rapid progress being made shows no sign of slackening.

Animals↗

Aspects of human parasites in which surgical intervention may be important.

Until recently, physicians and surgeons in developed countries only occasionally encountered patients with parasitic protozoan and helminthic infections. High-speed travel, immigration and the popularity of the tropics as vacation areas have increased the number of people at risk for parasitic disease. This chapter examines the significant literature on a select number of protozoan and helminthic parasites for which surgical intervention is important in the diagnosis, treatment or cure of the disease. Although traditional surgical approaches are covered, emphasis is placed on recent advances in the areas of transplantation and minimally invasive surgery. Combining the disciplines of parasitology and surgery, this chapter covers three protozoan and seven helminthic parasites for which surgery is a valid treatment option based on the frequency of cases reported in the literature. Following coverage of the selected parasites, a table is included listing additional helminths for which surgery contributes to patient management. Physicians in the USA, UK, and Europe need to be more aware of the presentation and treatment of parasitic infections. It is our sincere hope that this review accomplishes that goal, and ultimately benefits the patients we serve.

Adolescent↗

The host-parasite relationship in neosporosis.

Neospora caninum is an apicomplexan parasite which invades many different cell types and tissues. It causes neosporosis, namely stillbirth and abortion in cattle and neuromuscular disease in dogs, and has been found in several other animal species. N. caninum is closely related to Toxoplasma gondii, and controversial opinions exist with respect to its phylogenetical status. Initially, two stages of N. caninum had been identified, namely asexually proliferating tachyzoites and bradyzoites. The sexually produced stage of this parasite, oocysts containing sporozoites, has been found only recently. In order to answer the many open questions regarding its basic biology and its relationship with the host, a number of diagnostic tools have been developed. These techniques are based on the detection of antibodies against parasites in body fluids, the direct visualization of the parasite within tissue samples by immunohistochemistry, or the specific amplification of parasite DNA by PCR. Other studies have been aiming at the identification of specific antigenic components of N. caninum, and the molecular and functional characterization of these antigens with respect to the cell biology of the parasite. Clearly, molecular approaches will also be used increasingly to elucidate the immunological and pathogenetic events during infection, but also to prepare potential new immunotherapeutic tools for future vaccination against N. caninum infection.

Animals↗

Parasitic nematodes, proteinases and transgenic plants.

Parasite proteinases have important functions in host-parasite interactions. Consequently, they have been investigated as targets for the control of both plant and animal parasites. Plant parasitic nematodes cause estimated annual losses to world agriculture of US$100 billion and, currently, their control often relies on highly toxic nematicides, with associated environmental risks. The potential of disrupting digestive proteinases for plant parasitic nematode control, via expression of proteinase inhibitors in transgenic plants, is summarized here by Catherine Lilley, Pauline Devlin, Peter Urwin and Howard Atkinson. They then consider whether the approach of expressing antinematode proteins in plants can be adapted for control of certain animal parasitic nematodes.

Animals↗

Helminth and protozoan gastrointestinal tract parasites in captive and wild-trapped African non-human primates.

The objective of this study was to investigate the gastro-intestinal (GIT) parasites commonly occurring in captive and wild-trapped (WT) non-human primates (baboons, vervets and Sykes) in Kenya and compare their prevalence. Three hundred and fifteen faecal samples were subjected to a battery of diagnostic tests, namely, direct smear, modified formal ether sedimentation, Kato thick smear, Harada-Mori techniques for parasite detection and culture to facilitate nematode larvae identification. Of these, 203 (64.4%) harboured helminths and 54 (17.1%) had protozoa. The helminth parasites comprised Strongyloides fulleborni 141 (44.8%), Trichuris trichuira 200 (63.5,%), Oesophagostomum sp. 48 (15.2%), Trichostrongylus sp. 73 (23.2%), Enterobius vermicularis 44 (14.0%), Schistosoma mansoni 4/92 (4.3%) and Streptopharagus sp. 68 (21.6%). Protozoan parasites consisted of Entamoeba coli 204 (64.8%), Balantidium coli 127 (40.3%) and Entamoeba histolytica 78 (24.8%). Both WT and colony-borne (CB) primates had similar species of parasites, but higher prevalences of protozoan infection were observed in CB baboons while helminth infections were relatively more common in WT primates. Some of the parasites observed in this study are reported to be zoonotic in various parasitological literatures. Chemoprophylaxis and other managerial practices were believed to be responsible for the lower worm prevalence in CB primates. Similar intervention against protozoa and other agents will not only improve primate health, but also increase safety to animal handlers and colony workers.

Animals↗

Integrated and biological control of parasites in organic and conventional production systems.

Organic and other non-intensive animal production systems are of growing importance in several countries worldwide. In contrast to conventional farms, parasite control on organic farms is affected by several of the prescribed changes in management e.g. access to the outdoors in the summer and in most countries, a ban on preventive medication, including use of anti-parasiticides. Organic animal production relies heavily on grazing, and pasture or soil related parasites are thus of major importance. Several studies in northern temperate climate have indicated that outdoor production of pigs, primarily sows, and laying hens results in heavier and more prevalent helminth infections compared to conventional intensive production under indoor conditions. In organic dairy cattle, parasitic gastroenteritis in heifers may be more prevalent. In a short to medium term perspective, integrated control may combine grazing management with biological control using nematophagous micro-fungi, selected crops like tanniferous plants and on conventional farms, limited use of anti-parasiticides. At present, the non-chemotherapeutic control of pasture related infections is based mainly on grazing management strategies. Preventive strategies, where young, previously unexposed stock, are turned out on parasite-free pastures, can be used for grazing first season dairy heifers and in all-in-all-out poultry production. Evasive strategies aim at avoiding disease producing infections of a contaminated area by moving to a clean area and may be relevant for ruminants and pigs. In cattle, effective control of nematodes can be achieved by repeated moves of the herd or alternate grazing with other species. High stocking rates seem to be an important risk factor. In pig production, the effect of paddock rotation on parasite infections is largely unknown and studies are warranted. Control of nematodes by larvae-trapping fungi, or perhaps in the future by egg-destroying fungi, looks promising for ruminants and certain monogastric animals but delivery systems and practical dosing regimes integrated with grazing management have to be developed. In conclusion, good prospects are expected for acceptable parasite control without a heavy reliance on anti-parasiticides through integration of the above mentioned procedures but future studies are needed to confirm their efficacy under practical farming conditions.

Animal Husbandry↗

Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites.

Host cell invasion by apicomplexan parasites requires coordinated interactions between cell surface adhesins and the parasite cytoskeleton. We have identified a complex of parasite proteins, including the actin binding protein aldolase, which specifically interacts with the C-terminal domains of several parasite adhesins belonging to the thrombospondin-related anonymous protein (TRAP) family. Binding of aldolase to the adhesin was disrupted by mutation of a critical tryptophan in the C domain, a residue that was previously shown to be essential for parasite motility. Our findings reveal a potential role for aldolase in connecting TRAP family adhesins with the cytoskeleton, and provide a model linking adhesion with motility in apicomplexan parasites.

Actin Cytoskeleton↗

Community structure of helminth parasites of the tuna, Euthynnus affinis, from the Visakhapatnam coast, Bay of Bengal.

An analysis is made of the community structure of the helminth parasites of the tuna Euthynnus affinis collected off the coast of Visakhapatnam, Bay of Bengal. The helminth fauna comprised 23 species, consisting of two monogeneans, 18 digeneans, one larval cestode, one nematode and one acanthocephalan. Didymozoids, represented by 14 species, were the dominant members of the parasite spectrum. The parasite assemblage is characterized by species richness as well as a high diversity. Most of the parasites found, the didymozoids in particular, were host specialists, exhibiting a high degree of host specificity. The fauna comprised three core species, four satellite species and many secondary species, with no potential for interaction among them but the degree of predictability is high in that each infracommunity comprised two or three core species superimposed by a few secondary species. Many host factors such as the varied diet, high vagility, long life span and endothermy appear to have contributed to the development of the species rich and diverse parasite communities in the tuna. There was evidence for a decrease in parasite density and an increase in diversity with increase in host size, indicating that host size has a profound influence on the component community structure.

Animals↗

Imported Opisthorchis viverrini and parasite infections from Thai labourers in Taiwan.

In order to determine the prevalence of intestinal parasites among labourers from Thailand in Taiwan, the stool samples from 1364 Thai labourers were examined by the formalin-ether concentration method and 18.0% were found to be infected with one or more parasites. The infection rates of hookworm, Opisthorchis viverrini, Strongyloides stercoralis, Enterobius vermicularis, Ascaris lumbricoides, Hymenolepis nana, Capillaria philippinensis, Schistosoma japonicum, Echinostoma sp., Entamoeba coli, Giardia lamblia, and Entamoeba histolytica, were 7.6%, 7.0%, 3.2%, 0.5%, 0.3%, 0.1%, 0.1%, 0.1%, 0.1%, 0.4%, 0.2%, and 0.1% respectively. The prevalence was highest among the 21-25 age group (24.8%). Among the 245 infected persons, 91% were infected with one parasite, 8% with two parasites and 1% with three parasites. The finding that parasitic infections are prevalent among Thai labourers demonstrates the need for control measures in foreign labourers in Taiwan and further studies to determine the susceptibility of O. viverrini to the snail hosts of Clonorchis sinensis.

Adult↗

Concomitant infections, parasites and immune responses.

Concomitant infections are common in nature and often involve parasites. A number of examples of the interactions between protozoa and viruses, protozoa and bacteria, protozoa and other protozoa, protozoa and helminths, helminths and viruses, helminths and bacteria, and helminths and other helminths are described. In mixed infections the burden of one or both the infectious agents may be increased, one or both may be suppressed or one may be increased and the other suppressed. It is now possible to explain many of these interactions in terms of the effects parasites have on the immune system, particularly parasite-induced immunodepression, and the effects of cytokines controlling polarization to the Th1 or Th2 arms of the immune response. In addition, parasites may be affected, directly or indirectly, by cytokines and other immune effector molecules and parasites may themselves produce factors that affect the cells of the immune system. Parasites are, therefore, affected when they themselves, or other organisms, interact with the immune response and, in particular, the cytokine network. The importance of such interactions is discussed in relation to clinical disease and the development and use of vaccines.

Animals↗